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BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(special issue CARAH):33-42, 2011

COMPARISON OF GROWTH RATES ESTIMATED BY OTOLITH READING OF Scorpaena porcus AND Scorpaena notata CAUGHT ON ARTIFICIAL AND NATURAL REEFS OF THE NORTHERN ADRIATIC SEA*

Giuseppe Scarcella**, Fabio Grati, Piero Polidori, Filippo Domenichetti and Luca Bolognini, Gianna Fabi

CNR - Istituto di Scienze Marine

(UOS di Ancona, Largo Fiera della Pesca, 60125 Ancona, Italy)

**Corresponding author: [email protected]

A B S T R A C T

Despite the high number of studies on fish assemblages associated with artificial reefs and offshore platforms, little information exists on the growth rates of fish living on artificial and natural substrates. Age and growth was determined throughout otolith reading on two commercial scorpionfishes ( Scorpaena porcus and Scorpaena notata ) caught in the surroundings of artificial structures (artificial reefs and gas platforms) and natural habitats. Von Bertalanffy growth parameters were calculated for each species separately for each site. Age of S. porcus and S. notata ranged from 0 to 8 years and from 0 to 16 years, respectively. Kimura test applied to Von Bertalanffy growth curves indicated that the individuals of both species inhabiting the artificial structures had higher growth parameters than those caught in the natural habitat. The presence of artificial habitats in the northern Adriatic Sea positively affects growth rates and growth performance of both species, likely for the greater prey availability in respect to the natural open sea.

R E S U M O

Apesar do elevado número de estudos sobre as assembléias de peixes associadas a recifes artificiais e plataformas offshore, existe pouca informação sobre as taxas de crescimento dos peixes que vivem em substratos artificiais e naturais. A idade e crescimento foram determinados pela leitura de otólitos em dois peixes escorpião comerciais ( Scorpaena porcus e Scorpaena notata ) capturados nas imediações de estruturas artificiais (recifes artificiais e plataformas de gás) e habitats naturais. Parâmetros de crescimento de von Bertalanffy foram calculadoss separadamente para cada espécie e cada local. A idade de Scorpaena porcus e Scorpaena notata variou entre 0 e 8 anos e 0 e 16 anos, respectivamente. O teste Kimura aplicado às curvas de crescimento de Bertalanffy indicaram que os indivíduos das duas espécies que habitam as estruturas artificiais tinham parâmetros de crescimento mais elevados do que dos capturados no habitat natural. A presença de habitats artificiais no norte do Mar Adriático afeta positivamente as taxas de crescimento e o desempenho de crescimento de ambas as espécies, provavelmente pela maior disponibilidade de presas em relação ao mar aberto natural.

Descriptors: Scorpaena porcus, Scorpanea notata , Age and growth, Natural reefs, Artificial structures, Adriatic Sea. Descritores: Scorpaena porcus, Scorpaena notata , Idade e crescimento, Recifes naturais, Estruturas artificiais, Mar Adriático.

INTRODUCTION

(S. porcus up to 25 cm TL and S. notata up to 20 cm Scorpaena porcus and Scorpaena notata , TL) and commonly found among rocks and seagrass commonly known as the black scorpionfish and the beds (FISHER et al., 1986). small red scorpionfish respectively, are distributed in S. porcus is a relatively slow-growing and the eastern Atlantic from the British Isles to Morocco short-lived fish, with a maximum life span of 11 years and throughout the Mediterranean to the Black Sea. (BRADAI; BOUAIN, 1988; JARDAS; PALLAORO, Both species are benthic, sedentary, of medium size 1992). Similarly, S. notata seems to grow slowly, but lives longer (16 years; SCARCELLA, 2010). ______In the northern Adriatic Sea, S. porcus is (*) Paper presented at the 9 th CARAH – International Conference on commonly found in coastal waters, while S. notata is Artificial Reefs and Related Aquatic Habitats on 8-13 November, more abundant in deeper waters offshore. Curitiba, PR, Brazil. 34 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(special issue CARAH), 2011

Despite their low commercial value, mainly terms of their age composition and growth rate due to their small size, S. porcus and S. notata play a estimated by otolith reading and by applying indirect crucial role in the hard-bottom ecosystems, methods to evaluate the reliability (accuracy) and representing two important reef-dwelling species reproducibility (precision) of the age estimates. attracted by artificial structures, such as artificial reefs and offshore gas platforms, and the rare rocky habitats MATERIAL AND METHODS of the Adriatic Sea (BOMBACE et al., 1994; FABI et al., 2004; CASELLATO; STEFANON, 2008). Many Specimens of black scorpionfish ( S. porcus ) artificial reefs have been built in the last two decades and small red scorpionfish ( S. notata ) were collected throughout the Mediterranean in order to enhance in the northern Adriatic Sea between July 2004 and local fish populations and to improve small scale- November 2008. The study area included both natural fisheries as a consequence of fish attraction and/or reefs/rocky outcrops and artificial structures such as production of new biomass (JENSEN, 2002). Indeed, artificial reefs located in coastal waters and offshore several studies report high fish density, rapid gas platforms (Fig. 1). Artificial reefs were located at colonization and high catch rates in areas where about 1-6 km from the coast, at depths ranging from 8 artificial reefs have been deployed (e.g. BOHNSACK; to 15 m. Offshore gas platforms were located at 36-52 SUTHERLAND, 1985; CARR; HIXON, 1997). This km offshore on sandy or sandy-mud bottom, in 35 to is more evident in areas far from natural hard 75 m depths. Natural reefs were located from the substrates, where artificial reefs can provide additional shoreline to around 100 km offshore. food and shelter to mitigate predation, as is the case of Sampling was carried out in close proximity the Adriatic Sea (BOMBACE et al., 1990, 1994; to both natural reefs and artificial structures using a FABI; FIORENTINI, 1994). Although offshore gas beam trawl with 40 mm cod-end mesh size and platforms have a different primary purpose, they act in trammel nets with a 70 mm stretched mesh size. Hauls a similar way to artificial reefs, concentrating fish performed with the beam trawl were randomly located throughout the water column (e.g. PAGE et al., 1999; over the whole sampling area. The beam trawl was STANLEY; WILSON, 2000; FABI et al., 2004). generally towed at about 10 km h -1 for 15-30 minutes Despite the great number of studies on the during daylight. Trammel nets were set at dusk and fish assemblages associated with artificial reefs and pulled in at dawn, for a mean fishing time of 12 h. off-shore platforms, little information exists on the Each specimen caught was measured for ecological performance of fish living on these Total Length (TL) to the nearest mm below. Both substrates, in terms of differentiation in age and sagittal otoliths were removed from each fish, cleaned growth patterns from those of natural areas (LOVE et and stored dry in numbered vials. Length-frequency al., 2007). distributions of S. porcus and S. notata caught at In this study the differences in growth natural reefs and artificial structures were compared parameters between the scorpionfish populations with each other using the two-sample Kolmogorov- sampled in their natural habitat (NR) and those living Smirnov test (SOKAL; ROHLF, 1995). in artificial structures (AS) have been analyzed in

Fig. 1. Map of northern Adriatic Sea with the sampling stations where Scorpaena porcus and Scorpaena notata were caught. SCARELLA ET AL.: SCORPIONFISH GROWTH IN ARTIFICIAL AND NATURAL REEFS 35

The otoliths were fully immersed in ethanol epoxy resin and sectioned transversally. The otolith and observed under a stereomicroscope at 25-40× sections were then polished with 0.05 m alumina magnification. Under reflected light, the nucleus and paste and read under reflected light following the same the opaque zones appeared as light rings and the procedure as mentioned above (Fig. 3). To compare translucent or hyaline zones as dark rings (Fig. 2). the readings of the two procedures as applied to This pattern was quite clear for S. porcus and also for otoliths of S. porcus and smaller specimens of S. the young specimens of S. notata , while the otoliths of notata , a representative sample of them was read larger specimens of S. notata required sectioning and directly as a whole and then sectioned. As the age grinding because the ring pattern was difficult to estimates arrived at were the same, the sectioning distinguish due to the considerable thickness of the practice was carried out only on the thick otoliths of otoliths. These otoliths were , therefore , embedded in larger (older) individuals of S. notata .

Fig. 2. Photomicrograph of the sagittal otolith of Scorpaena porcus , showing the annulation pattern in a five years old female. Scale bar = 1 mm; first annulus ( black dot ); reading/measurement radius (black arrow ).

Fig. 3. Photographs of (a) surface and (b) cross- section otolith of Scorpaena notata , 16-years- old female, 165 mm total length (TL). Vertical line indicate plane observed by cross-section. Dots denote annulus from 1st to 16th.

36 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(special issue CARAH), 2011

The combination of each opaque and the micro-increments counted under a light subsequent translucent zone was considered to form an microscope at 400× and 630× magnification. annulus, as observed in other scorpaenids (MASSUTÍ The von Bertalanffy growth function was et al., 2000; LÓPEZ ABELLÁN et al., 2001; LA fitted to the estimated age-length data set taking into MESA et al., 2005). account the same size range and using the program Each otolith was read by one reader, without FISHPARM of the statistical package FSAS (SAILA any ancillary data on fish size. A second reading was et al., 1988), applying the Marquardt algorithm for carried out a week later by the same reader. When non-linear least square parameter estimation. The von readings differed by one or more years, a third reading Bertalanffy growth parameters (L ∞, k and t 0) were was made; if the difference persisted, the otolith was calculated for each population of each species sampled discarded. The index of Average Percentage Error in natural reefs and artificial structures, respectively, (APE) (BEAMISH; FOURNIER, 1981) and the mean and compared by the likelihood ratio test (KIMURA, Coefficient of Variation (CV) (CHANG, 1982) were 1980). A Student t test was employed to verify the calculated to estimate the relative precision of the differences between length-at-age data derived from readings. the Von Bertalanffy growth curves. To validate the seasonality of deposition of opaque and translucent zones, marginal increment RESULTS analysis was carried out on the entire otolith sample (SECOR et al., 1995; PANFILI et al., 2002). Since the Length Frequency Distributions spawning season of both species takes place between June and August (MUÑOZ et al., 2005), we The length frequency distributions of S. considered 1st July as the birthdate of the species. We porcus and S. notata populations caught on NR and observed that the opaque nucleus was deposited during AS are summarized in Fig. 4. As concerns the black the first summer after hatching, followed by the first scorpionfish, 138 specimens between 110-221 mm TL translucent zone laid down in the following winter just were caught on the NR, while 283 specimens between prior to the first birthday. Assuming that the annuli 80-270 mm TL were caught on AS. As regards the were added yearly, the age of the fish was estimated small red scorpionfish, 160 specimens between 47-180 by counting all the translucent zones. mm TL were caught on the NR and 378 specimens To validate specimens aged 0 years, i.e. fish between 95-199 mm TL on AS. with sagittae only composed of an opaque nucleus, No comparison between length frequency some otoliths were prepared for the counting of micro - distributions presented any statistical differences increments, assuming they are laid down daily (Kolmogorov-Smirnov test p<0.01). In particular, (LAIDIG; RALSTON, 1995; MASSUTÍ et al., 2000). specimens of S. porcus and S. notata caught on AS The otoliths were set in moulds, embedded in epoxy were larger than those observed on NR (Fig. 4). resin and ground until the sagittal plane was reached. They were polished with 0.05 m alumina paste and

Fig. 4. Length frequency distributions of Scorpaena porcus and Scorpaena notata from natural reefs (white) and artificial structures (grey) in the northern Adriatic Sea.

SCARELLA ET AL.: SCORPIONFISH GROWTH IN ARTIFICIAL AND NATURAL REEFS 37

Age Estimates, Accuracy and Precision age-length keys (Tables 1 and 2). Age distributions and longevity were comparable as between the The age composition estimated for each different populations of S. porcus and S. notata . species caught on the NR and AS is summarized in the

Table 1. Age-length keys of Scorpaena porcus from artificial structures and natural reefs in the northern Adriatic Sea

ArtificialArtificial structures Natural reefs Age (years ) 0 1 2 3 4 5 6 7 8 0 1 2 3 4 5 6 7 TL(mm) 80 1 85 90 95 1 100 105 1 110 1 2 1 115 1 120 1 3 3 125 4 4 2 3 3 1 130 1 2 2 1 1 2 135 1 1 1 1 2 3 1 140 3 1 2 2 4 2 1 145 1 4 2 1 1 4 5 150 4 6 1 1 2 3 1 155 2 4 4 3 5 160 4 5 5 2 1 4 1 2 165 7 2 3 7 5 170 5 8 7 6 7 175 1 8 5 1 2 3 1 1 180 1 5 4 4 1 2 4 1 185 5 7 7 1 1 1 2 2 190 2 6 3 2 1 2 1 195 3 10 9 2 1 2 4 200 3 4 5 8 2 4 205 2 7 1 1 2 1 1 210 6 1 3 1 1 1 1 1 215 3 3 2 2 1 220 3 2 2 1 1 1 225 1 1 230 2 2 1 235 2 240 245 1 1 1 250 1 2 2 1 255 2 1 260 1 265 1 1 270 1 38 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(special issue CARAH), 2011

Table 2. Age-length keys of Scorpaena notata from artificial structures and natural reefs in the northern Adriatic Sea.

Artificial Natural

structures reefs Age (years ) 1 1 2 3 4 5 67 8 9 10 11 12 13 14 16 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 TL(mm) 45 1 50 55 60 65 1 70 75 2 2 80 7 2 85 2 4 90 5 10 1 95 1 2 12 1 100 1 9 5 5 105 7 6 4 110 1 1 4 5 10 2 115 1 2 8 8 13 4 1 120 4 2 1 4 11 16 3 1 1 1 125 1 6 1 1 14 16 7 1 1 1 130 1 4 4 1 12 15 8 3 1 3 2 1 135 5 8 2 1 4 8 9 1 1 1 1 140 5 4 1 1 11 8 1 2 2 3 2 1 145 3 9 1 1 11 3 8 3 1 2 150 1 8 4 2 2 3 6 2 1 1 1 155 2 6 3 1 2 1 1 1 2 1 2 1 1 1 160 1 2 4 1 2 2 1 1 2 2 1 1 1 165 1 8 3 11 2 1 1 1 2 1 170 1 1 1 1 1 1 1 1 175 2 1 1 2 1 1 180 2 1 1 1 1 1 185 1 1 190 195 1

The annual periodicity of annulus deposition to 3.6 m in S. notata was observed from the core was corroborated by the marginal increment analysis, outward to the otolith margin. Age estimates were indicating that each pair of translucent and opaque from 240 to 350 days for S. porcus and from 140 to zones was formed over the course of a year. The 300 days for S. notata , thus validating specimens aged opaque zone was deposited from February to August 0 years, namely those having sagittae with an opaque in S. porcus and from April to August in S. notata . For nucleus and a more or less developed translucent zone. each species, the micro-increment counts to validate The reliability of the criteria used for fish aged 0 years (i.e. young of the year) on the basis judging the age of the two species was corroborated by of the annuli were carried out on five specimens the relatively high precision of the age readings. The randomly selected from the sample of fish caught on count of the variability indices APE and CV was lower the NR and the AS. The otolith microstructure showed for S. notata (8.2 and 11.6%, respectively), than for S. the typical pattern of alternating light and dark porcus (9.8 and 13.9%, respectively), with a increments, representing daily growth rings. A percentage agreement between readings of 56% for S. continuous series of concentric rings of increasing size porcus and 62% for S. notata , indicating a reasonable ranging from 1.2 to 2.8 m in S. porcus and from 1.0 consistency (or reproducibility) between readings. SCARELLA ET AL.: SCORPIONFISH GROWTH IN ARTIFICIAL AND NATURAL REEFS 39

Growth Rate notata alone when each parameter was considered separately (Table 4). No statistical differences in In order to compare the growth rates of length-at-age data derived from the Von Bertalanffy populations from different areas, the Von Bertalanffy growth curves (Table 5) were observed as between the parameters were computed and growth curves were two groups (NR and AS) of S. porcus (t-test for paired fitted to age-length data pairs estimated for natural and comparison, df = 8, p>0.5), principally due to the artificial structures, with reference to the same size similar growth patterns in the younger specimens. On range (Fig. 5; Table 3). The likelihood ratio test the other hand, the comparison between the two indicated that for both species the overall Von groups (NR and AS; Table 5) was significant for S. Bertalanffy growth curves differed significantly notata (t-test for paired comparison, df = 16, p<0.05). between the two groups (NR and AS), as well as for S.

Fig. 5. Plot of Von Bertalanffy growth curves for natural reefs (dotted line) and artificial strucutres (solid line) populations of Scorpaena porcus and Scorpaena notata from the northern Adriatic Sea.

Table 3. Estimates of Von Bertalanffy growth parameters and growth performance of Scorpaena porcus and Scorpaena notata from artificial structures and natural reefs in the northern Adriatic Sea.

Scorpaena porcus Scorpaena notata Natural Natural Artificial structures Artificial structures reefs reefs

L∞ (cm) 21.16 21.80 16.80 14.37 k (year -1) 0.43 0.29 0.48 0.30

t0 (year) -1.51 -2.51 -1.37 -2.85 Ф’ 2.29 2.14 2.13 1.84 n 255 138 159 341 n, sample size.

40 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 59(special issue CARAH), 2011

Table 4. Likelihood ratio test comparison of Von Bertalanffy parameters estimated for Scorpaena porcus and Scorpaena notata sampled from artificial structures (AS) and natural reefs (NR) in the northern Adriatic Sea. Scorpaena porcus Scorpaena notata Log residual Log residual Null hypothesis d.f. sum of χ2 sum of χ2 squares squares

L∞AS = L ∞NR 1 1.277 0.258 23.577 0.001** k AS = k NR 1 6.873 0.032* 7.466 0.028* t0 AS = t 0 NR 1 0.078 0.781 8.337 0.011*

L∞ AS , k AS , t 0 AS = L ∞ NR , k NR , t 0 NR 3 17.563 0.001** 208.730 0.001** d.f. = degree of freedom; * = significant at α = 0.05; ** = significant at α = 0.01

Table 5. Estimated values of fish length-at-age of Scorpaena porcus and Scorpaena notata from artificial structures and natural reefs derived from the Von Bertalanffy equations in the northern Adriatic Sea.

Scorpaena porcus Scorpaena notata artificial structures natural reefs artificial structures natural reefs Age TL (cm) TL (cm) TL (cm) TL (cm) 0 11.27 10.16 8.05 8.75 1 13.92 14.02 11.36 10.44 2 15.90 16.53 13.42 11.70 3 17.39 18.15 14.70 12.64 4 18.50 19.21 15.49 13.34 5 19.33 19.89 15.99 13.86 6 19.95 20.34 16.30 14.25 7 20.42 20.63 16.49 14.53 8 20.76 20.81 16.61 14.75 9 16.68 14.91 10 16.72 15.02 11 16.75 15.11 12 16.77 15.18 13 16.78 15.23 14 16.79 15.26 15 16.79 15.29 16 16.80 15.31

CONCLUSIONS Consistent with findings related to many other scorpaenids, such as Helicolenus dactylopterus The otoliths of the Scorpaenidae family are (MASSUTÍ et al., 2000), Scorpaena guttata (LOVE et characterized by relatively large size (TUSET et al., al., 1987), Scorpaena maderensis (LA MESA et al., 2008), making them easy to handle for the 2005) and Sebastes spp. (LOVE et al., 1990), the measurement of age. The inner structure of the sagittal results of the present study showed that the annuli in otoliths of S. porcus and S. notata closely resembled the sagittal otoliths of S. porcus and S. notata are laid those observed in other scorpaenids, with alternating down annually, the opaque zone being generally patterns of translucent and opaque zones around an deposited in spring-summer and the translucent zone opaque nucleus. The seasonal trend of the formation of in autumn-winter (MORALES-NIN, 2001). Moreover, the opaque zone accompanied the pattern of sea the great consistency among repeated age readings bottom temperature closely (ARTEGIANI et al., makes otoliths the most reliable basis for ageing 1997). scorpaenid fish.

SCARELLA ET AL.: SCORPIONFISH GROWTH IN ARTIFICIAL AND NATURAL REEFS 41

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